Systemic lack of canonical histamine receptor signaling results in increased resistance to autoimmune encephalomyelitis

Journal of Immunology

Volumn 191, Issue 2, 2013, Pages 614-622

  Saligrama, Naresha ^a   Case, Laure K ^a   Del Rio, Roxana ^a   Noubade, Rajkumar ^a   Teuscher, Cory ^a,b  

^a UNIVERSITY OF VERMONT COLLEGE OF MEDICINE   (United States)

^b UNIVERSITY OF VERMONT   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CYTOKINE; G PROTEIN COUPLED RECEPTOR; GLYCOPROTEIN GP 35 55; HISTAMINE H1 RECEPTOR; HISTAMINE H2 RECEPTOR; HISTAMINE H3 RECEPTOR; HISTAMINE H4 RECEPTOR; HISTAMINE RECEPTOR; HISTIDINE DECARBOXYLASE; MYELIN OLIGODENDROCYTE GLYCOPROTEIN; UNCLASSIFIED DRUG;

ADOPTIVE TRANSFER; ALLERGIC DISEASE; ALLERGIC ENCEPHALOMYELITIS; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIGEN PRESENTING CELL; ARTICLE; AUTOIMMUNE DISEASE; BLOOD BRAIN BARRIER; CELL ACTIVITY; CONTROLLED STUDY; CYTOKINE PRODUCTION; DISEASE PREDISPOSITION; DISEASE RESISTANCE; DISEASE SEVERITY; EFFECTOR CELL; ENZYME DEFICIENCY; IMMUNE RESPONSE; IMMUNIZATION; INTRACELLULAR SIGNALING; MOLECULAR MECHANICS; MOUSE; MULTIPLE SCLEROSIS; NEUROTRANSMISSION; NONHUMAN; PATHOGENESIS; PRIORITY JOURNAL; PROTEIN DEFICIENCY; PROTEIN FUNCTION; REGULATORY MECHANISM; REGULATORY T LYMPHOCYTE; SPLEEN CELL; T LYMPHOCYTE; TH1 CELL; TH17 CELL;

ANIMALS; ANTIGEN-PRESENTING CELLS; BLOOD-BRAIN BARRIER; CD4-POSITIVE T-LYMPHOCYTES; CELL DIFFERENTIATION; CELLS, CULTURED; CYTOKINES; ENCEPHALOMYELITIS, AUTOIMMUNE, EXPERIMENTAL; HISTAMINE; HISTIDINE DECARBOXYLASE; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MULTIPLE SCLEROSIS; MYELIN-OLIGODENDROCYTE GLYCOPROTEIN; PEPTIDE FRAGMENTS; RECEPTORS, HISTAMINE; SIGNAL TRANSDUCTION;

EID: 84880099354     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1203137     Document Type: Article

References (56)

1. Parsons, M. E., and C. R. Ganellin. 2006. Histamine and its receptors. Br. J. Pharmacol. 147(Suppl 1): S127-S135. (Pubitemid 43077270)
2. Akdis, C. A., and F. E. Simons. 2006. Histamine receptors are hot in immunopharmacology. Eur. J. Pharmacol. 533: 69-76. (Pubitemid 43340005)
3. Metcalfe, D. D., D. Baram, and Y. A. Mekori. 1997. Mast cells. Physiol. Rev. 77: 1033-1079. (Pubitemid 27459579)
4. Saligrama, N., R. Noubade, L. K. Case, R. del Rio, and C. Teuscher. 2012. Combinatorial roles for histamine H1-H2 and H3-H4 receptors in autoimmune inflammatory disease of the central nervous system. Eur. J. Immunol. 42: 1536-1546.
5. El Behi, M., S. Dubucquoi, D. Lefranc, H. Zéphir, J. De Seze, P. Vermersch, and L. Prin. 2005. New insights into cell responses involved in experimental autoimmune encephalomyelitis and multiple sclerosis. Immunol. Lett. 96: 11-26. (Pubitemid 39600755)
6. Logothetis, L., I. A. Mylonas, S. Baloyannis, M. Pashalidou, A. Orologas, A. Zafeiropoulos, V. Kosta, and T. C. Theoharides. 2005. A pilot, open label, clinical trial using hydroxyzine in multiple sclerosis. Int. J. Immunopathol. Pharmacol. 18: 771-778.
7. Alonso, A., S. S. Jick, and M. A. Hernán. 2006. Allergy, histamine 1 receptor blockers, and the risk of multiple sclerosis. Neurology 66: 572-575. (Pubitemid 43739890)
8. Lock, C., G. Hermans, R. Pedotti, A. Brendolan, E. Schadt, H. Garren, A. Langer-Gould, S. Strober, B. Cannella, J. Allard, et al. 2002. Gene-microarray analysis of multiple sclerosis lesions yields new targets validated in autoimmune encephalomyelitis. Nat. Med. 8: 500-508. (Pubitemid 34546753)
9. Pedotti, R., J. J. De Voss, L. Steinman, and S. J. Galli. 2003. Involvement of both 'allergic' and 'autoimmune' mechanisms in EAE, MS and other autoimmune diseases. Trends Immunol. 24: 479-484. (Pubitemid 37088150)
10. Bebo, B. F., Jr., T. Yong, E. L. Orr, and D. S. Linthicum. 1996. Hypothesis: a possible role for mast cells and their inflammatory mediators in the pathogenesis of autoimmune encephalomyelitis. J. Neurosci. Res. 45: 340-348. (Pubitemid 26299589)
11. Gregory, G. D., A. Bickford, M. Robbie-Ryan, M. Tanzola, and M. A. Brown. 2005. MASTering the immune response: mast cells in autoimmunity. Novartis Found. Symp. 271: 215-225, discussion 225-231.
12. Emerson, M. R., D. M. Orentas, S. G. Lynch, and S. M. LeVine. 2002. Activation of histamine H2 receptors ameliorates experimental allergic encephalomyelitis. Neuroreport 13: 1407-1410.
13. Musio, S., B. Gallo, S. Scabeni, M. Lapilla, P. L. Poliani, G. Matarese, H. Ohtsu, S. J. Galli, R. Mantegazza, L. Steinman, and R. Pedotti. 2006. A key regulatory role for histamine in experimental autoimmune encephalomyelitis: disease exacerbation in histidine decarboxylase-deficient mice. J. Immunol. 176: 17-26. (Pubitemid 43023244)
14. Fletcher, J. M., S. J. Lalor, C. M. Sweeney, N. Tubridy, and K. H. Mills. 2010. T cells in multiple sclerosis and experimental autoimmune encephalomyelitis. Clin. Exp. Immunol. 162: 1-11.
15. Noubade, R., G. Milligan, J. F. Zachary, E. P. Blankenhorn, R. del Rio, M. Rincon, and C. Teuscher. 2007. Histamine receptor H1 is required for TCR-mediated p38 MAPK activation and optimal IFN-gamma production in mice. J. Clin. Invest. 117: 3507-3518. (Pubitemid 350097006)
16. Teuscher, C., M. E. Poynter, H. Offner, A. Zamora, T. Watanabe, P. D. Fillmore, J. F. Zachary, and E. P. Blankenhorn. 2004. Attenuation of Th1 effector cell responses and susceptibility to experimental allergic encephalomyelitis in histamine H2 receptor knockout mice is due to dysregulation of cytokine production by antigen-presenting cells. Am. J. Pathol. 164: 883-892. (Pubitemid 38235470)
17. Teuscher, C., M. Subramanian, R. Noubade, J. F. Gao, H. Offner, J. F. Zachary, and E. P. Blankenhorn. 2007. Central histamine H3 receptor signaling negatively regulates susceptibility to autoimmune inflammatory disease of the CNS. Proc. Natl. Acad. Sci. USA 104: 10146-10151. (Pubitemid 47175277)
18. del Rio, R., R. Noubade, N. Saligrama, E. H. Wall, D. N. Krementsov, M. E. Poynter, J. F. Zachary, R. L. Thurmond, and C. Teuscher. 2012. Histamine H4 receptor optimizes T regulatory cell frequency and facilitates anti-inflammatory responses within the central nervous system. J. Immunol. 188: 541-547.
19. Ma, R. Z., J. Gao, N. D. Meeker, P. D. Fillmore, K. S. Tung, T. Watanabe, J. F. Zachary, H. Offner, E. P. Blankenhorn, and C. Teuscher. 2002. Identification of Bphs, an autoimmune disease locus, as histamine receptor H1. Science 297: 620-623. (Pubitemid 34815349)
20. Zampeli, E., and E. Tiligada. 2009. The role of histamine H4 receptor in immune and inflammatory disorders. Br. J. Pharmacol. 157: 24-33.
21. Ringstad, N., N. Abe, and H. R. Horvitz. 2009. Ligand-gated chloride channels are receptors for biogenic amines in C. elegans . Science 325: 96-100.
22. Hatton, G. I., and Q. Z. Yang. 2001. Ionotropic histamine receptors and H2 receptors modulate supraoptic oxytocin neuronal excitability and dye coupling. J. Neurosci. 21: 2974-2982. (Pubitemid 32323478)
23. Saras, A., G. Gisselmann, A. K. Vogt-Eisele, K. S. Erlkamp, O. Kletke, H. Pusch, and H. Hatt. 2008. Histamine action on vertebrate GABAA receptors: direct channel gating and potentiation of GABA responses. J. Biol. Chem. 283: 10470-10475.
24. Banu, Y., and T. Watanabe. 1999. Augmentation of antigen receptor-mediated responses by histamine H1 receptor signaling. J. Exp. Med. 189: 673-682. (Pubitemid 29193368)
25. Hofstra, C. L., P. J. Desai, R. L. Thurmond, and W. P. Fung-Leung. 2003. Histamine H4 receptor mediates chemotaxis and calcium mobilization of mast cells. J. Pharmacol. Exp. Ther. 305: 1212-1221. (Pubitemid 36618001)
26. Ohtsu, H., S. Tanaka, T. Terui, Y. Hori, Y. Makabe-Kobayashi, G. Pejler, E. Tchougounova, L. Hellman, M. Gertsenstein, N. Hirasawa, et al. 2001. Mice lacking histidine decarboxylase exhibit abnormal mast cells. FEBS Lett. 502: 53-56. (Pubitemid 32722059)
27. Teuscher, C., R. Noubade, K. Spach, B. McElvany, J. Y. Bunn, P. D. Fillmore, J. F. Zachary, and E. P. Blankenhorn. 2006. Evidence that the Y chromosome influences autoimmune disease in male and female mice. Proc. Natl. Acad. Sci. USA 103: 8024-8029. (Pubitemid 43801046)
28. Jutel, M., T. Watanabe, S. Klunker, M. Akdis, O. A. Thomet, J. Malolepszy, T. Zak-Nejmark, R. Koga, T. Kobayashi, K. Blaser, and C. A. Akdis. 2001. Histamine regulates T-cell and antibody responses by differential expression of H1 and H2 receptors. Nature 413: 420-425. (Pubitemid 32928596)
29. Codarri, L., G. Gyülvészi, V. Tosevski, L. Hesske, A. Fontana, L. Magnenat, T. Suter, and B. Becher. 2011. RORγt drives production of the cytokine GM-CSF in helper T cells, which is essential for the effector phase of autoimmune neuroinflammation. Nat. Immunol. 12: 560-567.
30. El-Behi, M., B. Ciric, H. Dai, Y. Yan, M. Cullimore, F. Safavi, G. X. Zhang, B. N. Dittel, and A. Rostami. 2011. The encephalitogenicity of T(H)17 cells is dependent on IL-1- and IL-23-induced production of the cytokine GM-CSF. Nat. Immunol. 12: 568-575.
31. Kroenke, M. A., S. W. Chensue, and B. M. Segal. 2010. EAE mediated by a non- IFN-γ/non-IL-17 pathway. Eur. J. Immunol. 40: 2340-2348.
32. Nakayama, T., Y. Kato, K. Hieshima, D. Nagakubo, Y. Kunori, T. Fujisawa, and O. Yoshie. 2004. Liver-expressed chemokine/CC chemokine ligand 16 attracts eosinophils by interacting with histamine H4 receptor. J. Immunol. 173: 2078-2083. (Pubitemid 38971645)
33. Liu, C., X. Ma, X. Jiang, S. J. Wilson, C. L. Hofstra, J. Blevitt, J. Pyati, X. Li, W. Chai, N. Carruthers, and T. W. Lovenberg. 2001. Cloning and pharmacological characterization of a fourth histamine receptor (H(4)) expressed in bone marrow. Mol. Pharmacol. 59: 420-426. (Pubitemid 32179918)
34. Hardie, R. C. 1989. A histamine-activated chloride channel involved in neurotransmission at a photoreceptor synapse. Nature 339: 704-706. (Pubitemid 19175354)
35. Karlin, A., and M. H. Akabas. 1995. Toward a structural basis for the function of nicotinic acetylcholine receptors and their cousins. Neuron 15: 1231-1244. (Pubitemid 26005363)
36. McCaman, R. E., and D. Weinreich. 1985. Histaminergic synaptic transmission in the cerebral ganglion of Aplysia. J. Neurophysiol. 53: 1016-1037. (Pubitemid 15085385)
37. Stuart, A. E. 1999. From fruit flies to barnacles, histamine is the neurotransmitter of arthropod photoreceptors. Neuron 22: 431-433. (Pubitemid 29159843)
38. Claiborne, B. J., and A. I. Selverston. 1984. Histamine as a neurotransmitter in the stomatogastric nervous system of the spiny lobster. J. Neurosci. 4: 708-721. (Pubitemid 14127181)
39. Sarthy, P. V. 1991. Histamine: a neurotransmitter candidate for Drosophila photoreceptors. J. Neurochem. 57: 1757-1768. (Pubitemid 21922816)
40. Pollack, I., and A. Hofbauer. 1991. Histamine-like immunoreactivity in the visual system and brain of Drosophila melanogaster. Cell Tissue Res. 266: 391-398.
41. Zheng, Y., B. Hirschberg, J. Yuan, A. P. Wang, D. C. Hunt, S. W. Ludmerer, D. M. Schmatz, and D. F. Cully. 2002. Identification of two novel Drosophila melanogaster histamine-gated chloride channel subunits expressed in the eye. J. Biol. Chem. 277: 2000-2005. (Pubitemid 34968780)
42. Fleck, M. W., J. L. Thomson, and L. B. Hough. 2012. Histamine-gated ion channels in mammals? Biochem. Pharmacol. 83: 1127-1135.
43. Wong, C. G., T. Bottiglieri, and O. C. Snead, III. 2003. GABA, gammahydroxybutyric acid, and neurological disease. Ann. Neurol. 54(Suppl 6): S3-S12. (Pubitemid 36903848)
44. Tian, J., Y. Lu, H. Zhang, C. H. Chau, H. N. Dang, and D. L. Kaufman. 2004. Gamma-aminobutyric acid inhibits T cell autoimmunity and the development of inflammatory responses in a mouse type 1 diabetes model. J. Immunol. 173: 5298-5304. (Pubitemid 39387814)
45. Reyes-García, M. G., F. Hernández-Hernández, B. Hernández-Téllez, and F. García-Tamayo. 2007. GABA (A) receptor subunits RNA expression in mice peritoneal macrophages modulate their IL-6/IL-12 production. J. Neuroimmunol. 188: 64-68. (Pubitemid 47095017)
46. Bergeret, M., M. Khrestchatisky, E. Tremblay, A. Bernard, A. Gregoire, and C. Chany. 1998. GABA modulates cytotoxicity of immunocompetent cells expressing GABAA receptor subunits. Biomed. Pharmacother. 52: 214-219. (Pubitemid 28305411)
47. Tian, J., C. Chau, T. G. Hales, and D. L. Kaufman. 1999. GABA(A) receptors mediate inhibition of T cell responses. J. Neuroimmunol. 96: 21-28. (Pubitemid 29179742)
48. Bjurstöm, H., J. Wang, I. Ericsson, M. Bengtsson, Y. Liu, S. Kumar-Mendu, S. Issazadeh-Navikas, and B. Birnir. 2008. GABA, a natural immunomodulator of T lymphocytes. J. Neuroimmunol. 205: 44-50.
49. Bhat, R., R. Axtell, A. Mitra, M. Miranda, C. Lock, R. W. Tsien, and L. Steinman. 2010. Inhibitory role for GABA in autoimmune inflammation. Proc. Natl. Acad. Sci. USA 107: 2580-2585.
50. Håkanson, R., L. I. Larsson, G. Liedberg, and F. Sundler. 1978. Evidence for H2- receptor-mediated feed-back regulation of histamine release from endocrine cells in the rat stomach. J. Physiol. 276: 151-157. (Pubitemid 8298518)
51. Håkanson, R., L. I. Larsson, G. Liedberg, J. F. Rehfeld, and F. Sundler. 1977. Suppression of rat stomach histidine decarboxylase activity by histamine: H2- receptor-mediated feed-back. J. Physiol. 269: 643-667. (Pubitemid 8156621)
52. Soldani, G., M. Garbarg, L. Intorre, S. Bertini, A. Rouleau, and J. C. Schwartz. 1996. Modulation of pentagastrin-induced histamine release by histamine H3 receptors in the dog. Scand. J. Gastroenterol. 31: 631-638. (Pubitemid 26290923)
53. Schneider, E., F. Machavoine, J. M. Pléau, A. F. Bertron, R. L. Thurmond, H. Ohtsu, T. Watanabe, A. H. Schinkel, and M. Dy. 2005. Organic cation transporter 3 modulates murine basophil functions by controlling intracellular histamine levels. J. Exp. Med. 202: 387-393. (Pubitemid 41126956)
54. Hrycay, E. G., and S. M. Bandiera. 2012. The monooxygenase, peroxidase, and peroxygenase properties of cytochrome P450. Arch. Biochem. Biophys. 522: 71-89.
55. Brandes, L. J., G. M. Queen, and F. S. LaBella. 2002. Displacement of histamine from liver cells and cell components by ligands for cytochromes P450. J. Cell. Biochem. 85: 820-824. (Pubitemid 34462791)
56. LaBella, F. S., and L. J. Brandes. 2000. Interaction of histamine and other bioamines with cytochromes P450: implications for cell growth modulation and chemopotentiation by drugs. Semin. Cancer Biol. 10: 47-53.